NOTES
AND
FIELD REPORTS
Appendix II. GenBank and photo voucher accession numbers.
An asterisk denotes sequences obtained from GenBank; all but
R35 for LAcrm were obtained from Weisrock and Janzen (2000).
Photo vouchers are not available for these GenBank specimens,
and this is indicated as NA. GenBank accession numbers are
given for cytochrome b, RAG-1, C-mos, and R35, respectively,
and separated by semicolons for each gene. Alleles for each gene
are separated by commas.
LAcr1m*
NA; AF168766*; DQ529173; DQ529206;
AY259581.1*
FLer1*
NA; AF168751*
GAsr*
NA; AF168752*
ONtr1*
NA; AF168757*
TXki*
NA; AF168759*
TXcc*
NA; AF168758*
TXsc*
NA; AF168760*; DQ529147, DQ529148;
DQ529185, DQ529186; DQ529125
NMrg*
NA; AF168756*; DQ529151; DQ529187;
DQ529127
MidCon63 ISUA200614; DQ529103; DQ529157, DQ529158;
DQ529192; DQ529122
TC34
ISUA200620; DQ529113
TC35
ISUA200621; DQ529112
TC37
ISUA200622; DQ529111
TC38
ISUA200623; DQ529114; DQ529132, DQ529133;
DQ529174; DQ529118
TC36
ISUA200625; EU040193; EU040200; EU040201,
EU040202; DQ529119
TC45
ISUA200624; EU040194; DQ529134, DQ529135;
DQ529175; no data R35
AM7
ISUA200717; EU040181
AMGst18 ISUA200716; EU040186
AMGst6
ISUA200714; EU040187
AMGst1
ISUA200713; EU040188
AMGst2
ISUA200712; EU040195
LT104
ISUA20073; EU040199
SM102
ISUA20075; EU040189
RM46
ISUA20077; EU040193
RM26
ISUA20079; ; EU040184
RM47
ISUA20076; EU040179
RM106
ISUA20074; EU040192
RM15
ISUA200715; EU040185
RC57
ISUA20078; EU040180
LG28
ISUA200718; EU040182
LIRim15
ISUA200710; EU040191
LGa46
ISUA20072; EU040190
LGa45
ISUA20071; EU040196
LGa25
ISUA200711; EU040197
LGaRim17 ISUA200719; EU040198
Chelonian Conservation and Biology, 2008, 7(1): 95–100
! 2008 Chelonian Research Foundation
Human Recreation and the Nesting Ecology
of a Freshwater Turtle (Chrysemys picta)
KENNETH D. BOWEN1,2
AND
FREDRIC J. JANZEN1
1
Department of Ecology, Evolution, and Organismal Biology, Iowa
State University, Ames, Iowa 50011 USA [fjanzen@iastate.edu];
2
Present Address: 13725 Shaftsburg Road, Perry, Michigan 48872
USA [kennethdbowen@gmail.com]
ABSTRACT. – Over a 3-year period, we studied the
relationship between the intensity of human recreation
95
and the nesting ecology of the painted turtle
(Chrysemys picta) at a major nesting beach. Our
results suggest that the intensity of human recreation
at this site had no effect on the decision of turtles to
emerge from the water and nest, or on habitat
selection by nesting turtles. This apparent lack of
effect of human recreation is contrary to the results of
many previously published studies on other taxa and
underscores the variability in wildlife responses to
human recreation and the need for species-specific and
population-specific studies.
The effects of human recreation on wildlife populations have recently received a great deal of scientific
attention, in part because of a rapid increase in outdoor
recreation activities over the last several decades (Flather
and Cordell 1995). To date, most reported effects of
recreation and human disturbance on wildlife have been
negative (Boyle and Samson 1985; Carney and Sydeman
1999). However, some investigators have suggested that
the effects of human disturbance on wildlife populations
may be overestimated (Boyle and Samson 1985; Nisbet
2000), and the impact of human recreation on groups such
as reptiles is not well studied (Boyle and Samson 1985).
Although declines in populations of organisms such
as amphibians (Wake 1991) have been well publicized,
concordant declines in turtle populations have received
comparatively little attention (Gibbons et al. 2000;
Klemens 2000). Although habitat alteration is a major
factor in turtle population declines (Mitchell and Klemens
2000), human recreation can also be detrimental (Garber
and Burger 1995; Bury and Luckenbach 2002). The
potential effects of human disturbance on the nesting
ecology of freshwater turtles are significant because
females may alter nest-site selection based on the risk
that they themselves will be depredated (Spencer 2002;
Spencer and Thompson 2003).
If females perceive humans as a predation risk and
alter their nesting behavior, maternal and offspring fitness
can be altered through combinations of a variety of factors.
For example, the site where a female chooses to deposit
eggs can affect the probability of nest depredation through
nest density (Valenzuela and Janzen 2001; Marchand et al.
2002; but see Burke et al. 1998) and edge effects (Temple
1987; Kolbe and Janzen 2002a). Nest-site selection may
also affect offspring survival through temperature-related
incubation success (Schwarzkopf and Brooks 1987;
Wilson 1998) and overwintering success (Weisrock and
Janzen 1999), as well as offspring sex ratio in turtles with
temperature-dependent sex determination (reviewed in
Bull 1983; Ewert and Nelson 1991; Janzen and Paukstis
1991; Shine 1999).
The purpose of this study was to determine the effects
of human recreation on the nesting behavior of the painted
turtle (Chrysemys picta). In particular, we evaluated how
different levels of human recreation on a major nesting
96
CHELONIAN CONSERVATION
AND
BIOLOGY, Volume 7, Number 1 — 2008
beach affected the decision of turtles to emerge from the
water and nest, as well as components of habitat selection
of nesting turtles. We hypothesized that an increased
number of humans on the nesting beach would decrease
the number of turtles emerging to nest and cause turtles to
choose low-quality nesting sites.
Methods. — This research represents a portion of a
long-term study of painted turtle nesting ecology (Janzen
1994) at the Thomson Causeway Recreation Area (TCRA)
near Thomson, Illinois. The Thomson Causeway is an
;450- 3 900-m island on the eastern bank of the
Mississippi River, and it contains an ;1.5-ha nesting area
that is bordered on the east side by a 200-m-wide slough
from which most turtles emerge to nest. The site is
managed and maintained by the United States Army Corp
of Engineers (USACE; see Kolbe and Janzen 2002a for a
more complete site description). The TCRA is a popular
destination for recreationists with motor homes (recreational vehicles [RV]) during the spring and summer
months. Use of the area is variable, with most activity
occurring on weekends and holidays (Bowen and Janzen,
pers. obs.). The nesting area is interspersed with concrete
pads for parking RVs and has a paved road running
through it. This setting provides an opportunity to
investigate the nesting responses of painted turtles to
different levels of human recreation throughout the nesting
season.
Chrysemys picta is a small- to medium-sized
freshwater turtle that ranges from southern Canada to
New Mexico and from the Atlantic to the Pacific Oceans
(Ernst et al. 1994; Starkey et al. 2003). At TCRA, the
mean clutch size is 10.5 6 2.0 standard deviation (SD)
eggs, and individual females may lay up to 3 clutches in a
nesting season from late May to early July (Morjan 2003).
Chrysemys picta has temperature-dependent sex determination, with cooler temperatures producing males (Ewert
and Nelson 1991). Hatchlings remain in the nest during the
winter and emerge from the nest and enter water in the
spring (Ernst et al. 1994; Weisrock and Janzen 1999).
The nesting beach at TCRA was monitored for
nesting turtles from early to late June in 2001 and from
late May to early July in 2002 and 2003. The turtles were
individually marked by using a series of notches in the
marginal scutes of the carapace (Cagle 1939). Each year
we observed females leave the water, construct nests, and
lay eggs. Once a female had finished nesting, we
temporarily mapped the location of the nest by using
nearby landmarks (e.g., trees, posts, and RV sites), and
determined the amount of overstory vegetation (% shaded)
in all 4 cardinal directions over the nest by using a
spherical densiometer (see Janzen 1994; Weisrock and
Janzen 1999). Once the nesting season was complete, we
returned to the location and established precise Cartesian
coordinates for each nest by using the program INTERPNT (Boose et al. 1998). Geographic information
system coverages were created by using these coordinates
in ArcViewt (ESRI Inc., Redlands, CA). We used these
location data to determine the distance of each nest from
the water. Error in this mapping and measuring process
ranges from 0 to 15 cm (see Kolbe and Janzen 2002a for
more detail). We also followed the fate of each nest
through the third week of September (i.e., until all
hatching was completed) by noting which nests had been
depredated and which remained intact.
As an indicator of the level of human disturbance at
TCRA during the nesting season, we used data on the
number of RVs present daily at the nesting beach and
nearby sites for the months of May through July in the
years 2001–2003 obtained from the USACE. We used
nested analysis of variance (ANOVA) to determine the
effect that varying numbers of RVs had on the decision of
turtles to nest. We used the number of nests constructed on
a given day as an indicator of the decision of turtles to
emerge from the water and nest. Effects in the nested
ANOVA were the number of RVs, the Julian date, and the
interaction between these two (all nested within year). The
Julian date was included in an attempt to control for
seasonal changes in nesting behavior that might be
independent of human activity.
We hypothesized that the number of turtles emerging
to nest would decrease as the number of RVs increased.
This relationship was considered important because mass
nesting events in response to decreased human presence
might increase nest density on small scales and serve as
cues for nest predators. Higher nest densities are known to
result in higher probabilities of nest depredation at TCRA
(Valenzuela and Janzen 2001).
We used nested ANOVAs to examine the effect of
human recreation on habitat selection of nesting turtles by
comparing the number of RVs present on a given day to
the distance from water of nests laid on that day and by
comparing the number of RVs present on a given day to
the south and west overstory vegetation cover of nests laid
on that day. Effects for each nested ANOVA were the
number of RVs, Julian date, maximum air temperature on
the day of nesting, water temperature on the day of
nesting, and the interactions between these variables (all
nested within year).
Weather variables were included in an attempt to
account for the effects of weather on habitat selection.
Maximum air temperature and water temperature were
chosen because these variables appear to affect the
decision of turtles to emerge from the water and nest at
TCRA (Bowen et al. 2005). We obtained weather data for
the nesting seasons from the USACE Lock and Dam 13,
ca. 12 km south of the study site.
We hypothesized that as the level of human activity
increased females would perceive a greater risk to
themselves, and the distance of nests from the water
would decrease (Spencer 2002). This relationship was
considered important because rates of nest depredation are
higher along the water edge in most years at TCRA (Kolbe
and Janzen 2002a). Sites near the water are less shaded at
TCRA; therefore, we hypothesized that nest overstory
NOTES
AND
FIELD REPORTS
97
Table 1. Descriptive statistics (mean 6 1 SD) and sample sizes for human recreational activity and nest variables of the painted turtle
(Chrysemys picta) at a nesting beach in northwestern Illinois.
Y (nests)
No. nests/d
Nest distance to water (m)
Nest southwest overstory vegetation (%)
RV/da
2001 (147)
2002 (158)
2003 (218)
7.1 6 7.6 (23 d)
7.7 6 9.3 (23 d)
6.6 6 7.3 (35 d)
34.3 6 24.6
28.6 6 23.6
24.7 6 23.0
39.2 6 21.0
42.8 6 22.6
41.7 6 22.4
5.6 6 9.1
18.3 6 13.8
23.6 6 19.0
a
recreational vehicle.
vegetation cover would decrease with increasing levels of
human recreation (Kolbe and Janzen 2002a). This
relationship was considered important because south and
west overstory vegetation cover is a predictor of nest
temperature and offspring sex ratio at this site in most
years (Janzen 1994; Morjan and Janzen 2003). Nesting
turtles are known to choose nesting sites nonrandomly
with respect to overstory vegetation at TCRA (Janzen and
Morjan 2001).
Although some females at TCRA lay multiple
clutches within a nesting season (Morjan 2003), we used
only the first nest for each female within years in our
analyses. We did so to ensure that each nesting event was
independent within years (i.e., females may exhibit
different nesting behavior during their second attempt,
based on what they experience during their first attempt).
Adding data from second and third nests did not change
our findings (results not shown). All statistical analyses
were performed by using JMP (SAS Institute Inc).
Results. — Nesting began by 7 June in each year and
the nesting beach was monitored until at least 1 July.
Either 23 (2001 and 2003) or 35 (2002) nesting days for
each year were included in the analyses. The number of
nesting days varied, in part, as a result of weather
conditions that inhibited nesting on some days. Data were
analyzed from 147 nests in 2001, 158 nests in 2002, and
218 nests in 2003. Nest parameters were highly variable
during the nesting season in all years studied, as was the
number of RVs present at TCRA (ranging from 0 to 64
RVs per day; Table 1). Overall, substantial within- and
among-year variation existed in the data set for the
response and predictor variables of interest in this study.
The number of nests laid on a given day was not
affected by any of the predictor variables (overall
Table 2. Results for individual effects from a nested analysis of
variance to determine the effect of the number of recreational
vehicles (RV) on the number of painted turtle (Chrysemys picta)
nests constructed on a nesting beach in northwestern Illinois
during the years 2001–2003.a An asterisk (*) signifies an
interaction between terms.
Source of variation
df
Sum of squares
F-ratio
p value
RVs
Julian date
RVs*Julian date
Y
3
3
3
2
100.49657
29.93952
80.81181
20.06618
0.5084
0.1515
0.4088
0.1523
0.6778
0.9284
0.7471
0.8590
a
All effects were nested within year. The p value and r 2 value for the
overall test were 0.7993 and 0.09, respectively.
p ¼ 0.7993, r2 ¼ 0.09; Table 2). A similar pattern was
observed for overstory vegetation (overall p ¼ 0.4360,
r2 ¼ 0.06; Table 3). The nested ANOVA for the distance
of the nests from water was statistically significant (overall
p ¼ 0.0009), but none of the individual effects approached
statistical significance and the r2 value was small
(r2 ¼ 0.12; Table 4). The biological significance, therefore,
is likely to be negligible.
Discussion. — Human recreational activity, as
measured by the number of RVs on and near a major
nesting beach, did not appear to affect large-scale patterns
in the nesting ecology of the population of painted turtles
studied here. Variables that represented both the decision
to emerge from the water to nest and habitat selection had
no biologically significant relationship with the number of
RVs present.
Based on the results of previous studies, the lack of
effect found here was unexpected. For example, breeding
and nest survival of colonial waterbirds may be negatively
affected by human recreation (Yorio et al. 2001; reviewed
in Carney and Sydeman 1999). Garber and Burger (1995)
documented that 2 populations of the wood turtle
(Glyptemys insculpta) declined 100% within 10 years
after the opening of habitat to human recreation (foot
traffic leading to opportunistic removal of turtles). Bury
and Luckenbach (2002) found that a population of desert
tortoises (Gopherus agassizii) that was subjected to human
recreation in the form of off-road vehicles appeared to be
less dense and less healthy than a population that was
protected. Given that human recreation and disturbance
can have adverse effects on breeding organisms in general
and on turtle populations in particular, combined with the
likelihood for some turtles to alter nesting behavior when
disturbed or when they perceive danger (Iverson and
Smith 1993; Spencer 2002; Spencer and Thompson 2003),
one might assume that nesting turtles would suffer from
human activity. It is important to note, however, that we
studied behavioral responses and not population dynamics.
Our results give tentative support to the assertion of a
number of investigators (Whittaker and Knight 1998;
Miller and Hobbs 2000; Nisbet 2000) that wildlife
responses to human recreation are difficult to generalize.
Wildlife may respond to human recreation in many ways,
thus studies of these effects should be done on a speciesspecific level (Miller and Hobbs 2000). A populationspecific level may be necessary if some species are capable
of habituating to disturbance by humans (i.e., they no
98
CHELONIAN CONSERVATION
AND
BIOLOGY, Volume 7, Number 1 — 2008
Table 3. Results for individual effects from a nested analysis of variance to determine the effect of the number of recreational vehicles
(RV) on the south and west overstory vegetation of painted turtle (Chrysemys picta) nests constructed on a nesting beach in
northwestern Illinois during the years 2001–2003.a
Source of variation
df
Sum of squares
F-ratio
p value
RVs
Julian date
Maximum air temperature
Water temperature
Y
RVs*Julian date
Maximum air temperature*water temperature
Julian date*water temperature
RVs*water temperature
Julian date*maximum air temperature
RVs*maximum air temperature
3
3
3
3
2
3
3
3
3
3
3
0.18924736
0.08643256
0.10417674
0.05369669
0.02290302
0.04975900
0.3947058
0.02635718
0.05441639
0.03492956
0.01753739
1.2962
0.5920
0.7135
0.3678
0.2353
0.3408
0.2703
0.1805
0.3727
0.2392
0.1201
0.2750
0.6205
0.5442
0.7763
0.7904
0.7958
0.8468
0.9096
0.7727
0.8690
0.9483
a
All effects were nested within year. The p value and r 2 value for the overall test were 0.4360 and 0.06, respectively. An asterisk (*) signifies an
interaction between terms.
longer respond to human disturbance; Whittaker and
Knight 1998). In the future, we plan to test the hypothesis
that our turtles have habituated to human presence by
using comparative experimental studies with nearby
populations.
There is an important caveat to consider in interpreting our results: the analytical methods used are capable of
detecting only large-scale changes in turtle nesting
behavior as a result of human recreation. We did not
evaluate the responses of individual turtles per se, nor did
we directly track population dynamics. We have observed
turtles abandon nesting attempts as the result of direct
human intrusion, adults and hatchlings killed by automobiles, and removal of turtles from the study area by
recreationists. These types of situations are not accounted
for in our analysis. Examining the response of an
individual turtle under different conditions might be more
instructive in determining the effects of human recreation.
However, this experimental approach would be difficult to
implement given that we cannot control when a turtle
emerges to nest nor can we directly manipulate the
intensity of human recreation.
What do our results mean for managers? Human
recreation at TCRA does not appear to have effects on
large-scale patterns of painted turtle nesting behavior, and
the needs of these turtles and human recreationists may be
reconcilable. However, we emphasize that these results
should not be taken to suggest that human recreation does
not affect freshwater turtles. Generalizations to other
species and other forms of recreation should be avoided.
Furthermore, even if painted turtles are unaffected by
large-scale human activity, the actions of individual
humans (removing or disturbing nesting turtles, road kills)
should still be taken into account. Education of the public
(Klein 1993; Taylor and Knight 2003) concerning the
plight and sensitivity of turtles is a good first step. At
TCRA, education over the past 15 years by both our
research team and USACE park rangers has minimized,
but not eliminated, individual human disturbance of
painted turtles. Monitoring and enforcement of applicable
laws will still be necessary in most cases.
We generally agree with other investigators (Boyle
and Samson 1985; Nisbet 2000) that the large number of
studies that suggest a negative relationship between human
recreation and wildlife should not be applied to all species
and all situations. Furthermore, studies that test explicit
hypotheses and attempt to determine the fitness effects of
recreation on wildlife (Boyle and Samson 1985) should be
Table 4. Results for individual effects from a nested analysis of variance to determine the effect of the number of recreational vehicles
(RV) on the distance from water of painted turtle (Chrysemys picta) nests constructed on a nesting beach in northwestern Illinois during
the years 2001–2003.a
Source of variation
df
Sum of squares
F-ratio
p value
RVs
Julian date
Maximum air temperature
Water temperature
Y
RVs*Julian date
Maximum air temperature*water temperature
Julian date*water temperature
RVs*water temperature
Julian date*maximum air temperature
RVs*maximum air temperature
3
3
3
3
2
3
3
3
3
3
3
1910.2945
1285.4191
462.8087
1089.7052
216.1942
2443.1515
778.8275
777.8249
756.6510
405.0941
545.6739
1.1771
0.7921
0.2852
0.6715
0.1998
1.5055
0.4799
0.4793
0.4662
0.2496
0.3362
0.3179
0.4987
0.8361
0.5699
0.8189
0.2123
0.6964
0.6968
0.7060
0.8616
0.7991
a
All effects were nested within year. The p value and r 2 value for the overall test were 0.0009 and 0.12, respectively. An asterisk (*) signifies an
interaction between terms.
NOTES
AND
FIELD REPORTS
designed where feasible. Finally, although research on
‘‘secure’’ populations of freshwater turtles is important
(Congdon et al. 2003), ecological and evolutionary studies
on human-influenced populations (Kolbe and Janzen
2002b; Feinberg and Burke 2003) are equally crucial
given the current rate of habitat alteration and the
conservation status of most turtle species. Future studies
should focus on the area around individual nesting turtles
that must be kept inviolate, if they are to remain
undisturbed (area of influence; Miller et al. 2001), and on
the effects of recreation-related deaths and adult removals
on population dynamics (Garber and Burger 1995).
Acknowledgments. — We thank the U.S. Army Corps
of Engineers for continued access to the field site and the
Janzen Lab turtle camp crews from 2001–2003 for helping
with data collection. E. Bowen, R. Brooks, J. Carr, W.
Clark, M. Haussmann, and R. Spencer provided comments
on earlier drafts of the manuscript. The research was
conducted under approved animal care protocols from
Iowa State University and by permission of the U.S. Fish
and Wildlife Service and the Illinois Department of
Natural Resources. Funding was provided by NSF grant
DEB0089680 to FJJ. KDB acknowledges the support of
an Iowa State University Graduate College Fellowship.
LITERATURE CITED
BOOSE, E.R., BOOSE, E.F., AND LEZBERG, A.L. 1998. A practical
method for mapping trees using distance measurements.
Ecology 79:819–827.
BOWEN, K.D., SPENCER, R.-J., AND JANZEN, F.J. 2005. A
comparative study of environmental factors that affect nesting
in Australian and North American freshwater turtles. Journal
of Zoology 267:397–404.
BOYLE, S.A. AND SAMSON, F.B. 1985. Effects of nonconsumptive
recreation on wildlife: a review. Wildlife Society Bulletin 13:
110–116.
BULL, J.J. 1983. Evolution of Sex Determining Mechanisms.
Menlo Park, CA: Benjamin/Cummings, 316 pp.
BURKE, V.J., RATHBUN, S.L., BODIE, J.R., AND GIBBONS, J.W. 1998.
Effect of density on predation rate for turtles in a complex
landscape. Oikos 83:3–11.
BURY, R.B. AND LUCKENBACH, R.A. 2002. Comparison of desert
tortoise (Gopherus agassizii) populations in an unused and
off-road vehicle area in the Mojave desert. Chelonian
Conservation and Biology 4:457–463.
CAGLE, F.R. 1939. A system of marking turtles for future
identification. Copeia 1939:170–173.
CARNEY, J.M. AND SYDEMAN, W.J. 1999. A review of human
disturbance effects on nesting colonial waterbirds. Waterbirds
22:68–79.
CONGDON, J.D., NAGLE, R.D., KINNEY, O.M., VAN LOBEN SELS,
R.C., QUINTER, T., AND TINKLE, D.W. 2003. Testing hypotheses
of aging in long-lived Painted Turtles (Chrysemys picta).
Experimental Gerontology 38:765–772.
ERNST, C.H., LOVICH, J.E., AND BARBOUR, R.W. 1994. Turtles of
the United States and Canada. Washington, D.C.: Smithsonian
Institution Press, 682 pp.
EWERT, M.A. AND NELSON, C.E. 1991. Sex determination in
99
turtles: diverse patterns and possible adaptive values. Copeia
1991:50–69.
FEINBERG, J.A. AND BURKE, R.L. 2003. Nesting ecology and
predation of Diamondback Terrapins, Malaclemys terrapin, at
Gateway National Recreation Area, New York. Journal of
Herpetology 37:517–526.
FLATHER, C.H. AND CORDELL, H.K. 1995. Outdoor recreation:
historical and anticipated trends. In: Knight, R.L. and
Gutzwiller, K.J. (Eds.). Wildlife and Recreationists: Coexistence through Management and Research. Washington, D.C.:
Island Press, pp. 3–16.
GARBER, S.D. AND BURGER, J. 1995. A 20-yr study documenting
the relationship between turtle decline and human recreation.
Ecological Applications 5:1151–1162.
GIBBONS, J.W., SCOTT, D.E., RYAN, T.J., BUHLMANN, K.A.,
TUBERVILLE, T.D., METTS, B.S., GREENE, J.L., MILLS, T., LEIDEN,
Y., POPPY, S., AND WINNE, C.T. 2000. The global decline of
reptiles, déjà vu amphibians. Bioscience 50:653–666.
IVERSON, J.B. AND SMITH, G.R. 1993. Reproductive ecology of the
Painted Turtle (Chrysemys picta) in the Nebraska sandhills
and across its range. Copeia 1993:1–21.
JANZEN, F.J. 1994. Vegetational cover predicts the sex ratio of
hatchling turtles in natural nests. Ecology 75:1593–1599.
JANZEN, F.J. AND MORJAN, C.L. 2001. Repeatability of microenvironment-specific nesting behaviour in a turtle with environmental sex determination. Animal Behaviour 62:73–82.
JANZEN, F.J. AND PAUKSTIS, G.L. 1991. Environmental sex
determination in reptiles: ecology, evolution and experimental
design. Quarterly Review of Biology 66:149–179.
KLEIN, M.L. 1993. Waterbird behavioral responses to human
disturbances. Wildlife Society Bulletin 21:31–39.
KLEMENS, M.W. 2000. Introduction. In: Klemens, M.W. (Ed.).
Turtle Conservation. Washington D.C.: Smithsonian Institution Press, pp. 1–4.
KOLBE, J.J. AND JANZEN, F.J. 2002a. Spatial and temporal
dynamics of turtle nest predation: edge effects. Oikos 99:
538–544.
KOLBE, J.J. AND JANZEN, F.J. 2002b. Impact of nest-site selection
on nest success and nest temperature in natural and disturbed
habitats. Ecology 83:269–281.
MARCHAND, M.N., LITVAITIS, J.A., MAIER, T.J., AND DEGRAAF,
R.M. 2002. Use of artificial nests to investigate predation on
freshwater turtle nests. Wildlife Society Bulletin 30:
1092–1098.
MILLER, J.R. AND HOBBS, N.T. 2000. Recreational trails, human
activity, and nest predation in lowland riparian areas.
Landscape and Urban Planning 50:227–236.
MILLER, S.G., KNIGHT, R.L., AND MILLER, C.K. 2001. Wildlife
responses to pedestrians and dogs. Wildlife Society Bulletin
29:124–132.
MITCHELL, J.C. AND KLEMENS, M.W. 2000. Primary and secondary
effects of habitat alteration. In: Klemens, M.W. (Ed.). Turtle
Conservation. Washington D.C.: Smithsonian Institution
Press, pp. 5–32.
MORJAN, C.L. 2003. Variation in nesting patterns affecting nest
temperatures in two populations of Painted Turtles
(Chrysemys picta) with temperature-dependent sex determination. Behavioral Ecology and Sociobiology 53:254–261.
MORJAN, C.L. AND JANZEN, F.J. 2003. Nest temperature is not
related to egg size in a turtle with temperature-dependent sex
determination. Copeia 2003:366–372.
NISBET, I.C.T. 2000. Disturbance, habituation, and management
of waterbird colonies. Waterbirds 23:312–322.
SCHWARZKOPF, L. AND BROOKS, R.J. 1987. Nest-site selection and
CHELONIAN CONSERVATION
100
AND
BIOLOGY, Volume 7, Number 1 — 2008
offspring sex ratio in Painted turtles, Chrysemys picta. Copeia
1987:53–61.
SHINE, R. 1999. Why is sex environmentally determined by nest
temperature in many reptiles? Trends in Ecology and
Evolution 14:186–189.
SPENCER, R.-J. 2002. Experimentally testing nest site selection:
fitness trade-offs and predation risk in turtles. Ecology 83:
2136–2144.
SPENCER, R.-J. AND THOMPSON, M.B. 2003. The significance of
predation in nest site selection of turtles: an experimental
consideration of macro- and microhabitat preferences. Oikos
102:592–600.
STARKEY, D.E., SHAFFER, H.B., BURKE, R.L., FORSTNER, M.R.J.,
IVERSON, J.B., JANZEN, F.J., RHODIN, A.G.J., AND ULTSCH, G.R.
2003. Molecular systematics, phylogeography, and the effects
of Pleistocene glaciation in the Painted Turtle (Chrysemys
picta) complex. Evolution 57:119–128.
TAYLOR, A.R. AND KNIGHT, R.L. 2003. Wildlife responses to
recreation and associated visitor perceptions. Ecological
Applications 13:951–963.
TEMPLE, S.A. 1987. Predation on turtle nests increases near
ecological edges. Copeia 1987:250–252.
VALENZUELA, N. AND JANZEN, F.J. 2001. Nest-site philopatry and
the evolution of temperature-dependent sex determination.
Evolutionary Ecology Research 3:779–794.
WAKE, D.B. 1991. Declining amphibian populations. Science
253:860.
WEISROCK, D.W. AND JANZEN, F.J. 1999. Thermal and fitnessrelated consequences of nest location in Painted Turtles
(Chrysemys picta). Functional Ecology 13:94–101.
WHITTAKER, D. AND KNIGHT, R.L. 1998. Understanding wildlife
responses to humans. Wildlife Society Bulletin 26:312–317.
WILSON, D.S. 1998. Nest-site selection: microhabitat variation
and its effects on the survival of turtle embryos. Ecology 79:
1884–1892.
YORIO, P., FRERE, E., GANDINI, P., AND SCHIAVINI, A. 2001.
Tourism and recreation at seabird breeding sites in Patagonia,
Argentina: current concerns and future prospects. Bird
Conservation International 11:231–245.
Received: 20 January 2006
Revised and Accepted: 30 May 2007
Chelonian Conservation and Biology, 2008, 7(1): 100–104
! 2008 Chelonian Research Foundation
Population Structure of the Alligator
Snapping Turtle, Macrochelys temminckii, on
the Western Edge of its Distribution
J. DAREN RIEDLE1,4, PAUL A. SHIPMAN1,5,
STANLEY F. FOX2, JOSEPH C. HACKLER1, AND
DAVID M. LESLIE, JR3
1
Oklahoma Cooperative Fish and Wildlife Research Unit,
Department of Zoology, Oklahoma State University, Stillwater,
Oklahoma 74078 USA [les_tortues@hotmail.com];
2
Department of Zoology, Oklahoma State University, Stillwater,
Oklahoma 74078 USA [foxstan@okstate.edu];
3
United States Geological Survey, Oklahoma Cooperative Fish and
Wildlife Research Unit, Oklahoma State University, Stillwater,
Oklahoma 74078 USA [cleslie@usgs.gov];
Present Address: Department of Life, Earth and Environmental
Sciences, West Texas A&M University, Canyon, Texas 79016 USA
[macrochelys@hotmail.com];
5
Present Address: Department of Biological Sciences, Rochester
Institute of Technology, 85 Lomb Memorial Drive, Rochester, New
York 14623 USA [passbi@rit.edu]
4
ABSTRACT. – A mark-recapture project on Macrochelys
temminckii was conducted between 1997 and 2000 at
Sequoyah National Wildlife Refuge, Muskogee and
Sequoyah counties, in eastern Oklahoma. Turtles were
captured in all streams and exhibited equal sex ratios,
marked sexual-size dimorphism, and population densities between 28 and 34 animals per km stretch of
stream. There was evidence of past population
perturbations, with very few large adults captured,
and a cohort of subadults highly underrepresented.
Turtles have long been recognized as an integral part
of aquatic communities, and all relevant literature on river
turtle diversity, ecological roles, and community structure
was recently reviewed in Moll and Moll (2004). Within this
synopsis though, it is clear that outside of common species,
such as the slider turtle, Trachemys scripta (Cagle 1950;
Gibbons 1990), in-depth life history studies of individual
species are noticeably absent. Detailed life-history strategies have been constructed only for a handful of species,
most notably the Blanding’s turtle, Emydoidea blandingii
(Congdon et al. 1993), and the common snapping turtle,
Chelydra serpentina (Congdon et al. 1994). The data
collected on C. serpentina were representative only of
populations at the northern reaches of the species’
distribution and so did not demonstrate geographic
variation in life-history strategies for that species. With
many species of turtles facing various threats, a better
understanding of these life-history strategies is much
needed for developing sound management strategies.
The alligator snapping turtle, Macrochelys temminckii, is a large, riverine, bottom-dwelling species that
occupies a predator-scavenger role in the southeastern
United States (Moll and Moll 2000). Shipman and Riedle
(1994) and Shipman and Neeley (1998) surveyed 2
populations in southeastern Missouri. In each, turtles were
2–24 kg in body mass; the sex ratio for the 2 populations
was 1 male to 1.09 females. Trauth et al. (1998) surveyed
2 sites in Arkansas with a population sex ratio of 1:1 and
reported that males were significantly larger than females.
Males were also significantly larger than females from
examination of specimens at a commercial meat-processing facility in Louisiana (Tucker and Sloan 1997). Based
on growth curves, M. temminckii reached sexual maturity
when the straight carapace length (CL) was 370 mm in
males and 330 mm in females (Dobie 1971; Tucker and
Sloan 1997).
Because of the apparent decline of the species
throughout its range (Pritchard 1989; Ernst et al. 1994),